Skip to main content

Species clarification of the prize medicinal Ganoderma mushroom “Lingzhi”

Abstract

“Lingzhi” is a mushroom that has been renowned in China for more than 2,000 years because of its claimed medicinal properties plus its symbolic fortune. “Lingzhi” has high economic value mostly as a dietary supplement in the modern market especially in East Asia, and its medicinal functions have become a hot study topic. For over a century, the highly prized medicinal fungus, known as “Lingzhi” in East Asia, has been assigned to Ganoderma lucidum, a species originally described from Europe. Molecular studies in recent years have revealed that the commercially cultivated ‘G. lucidum’ (“Lingzhi”) in East Asia is a different species from the true G. lucidum. The present study aims to clarify the species identity of “Lingzhi” based on morphological studies and analysis of rDNA nuc-ITS sequences, and additional gene fragments of mt-SSU, RPB1, RPB2, and TEF1-α of “Lingzhi” were provided. All Ganoderma species that mostly resemble “Lingzhi” in phylogeny and /or morphology were included for analysis. We propose a new species G. lingzhi for “Lingzhi”, which has an East Asia distribution. The most striking characteristics which differentiate G. lingzhi from G. lucidum are the presence of melanoid bands in the context, a yellow pore surface and thick dissepiments (80–120 μm) at maturity. G. curtisii is most closely related to G. lingzhi in phylogeny and is from North America. Ganoderma flexipes, G. multipileum, G. sichuanense, G. tropicum and ‘G. tsugae, are also closely related with G. lingzhi and are reported from China. These species are compared and discussed. ‘Ganoderma tsuage’ reported from China is determined as conspecific with G. lucidum, hence the distribution of G. lucidum extends from Europe to northeastern China.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Aly AH, Debbab A, Proksch P (2011) Fifty years of drug discovery from fungi. Fungal Divers 50:3–19

    Article  Google Scholar 

  2. Anonymous (1969) Flora of British fungi. Colour identification chart. Her Majesty´s Stationery Office, London

    Google Scholar 

  3. Bao XF, Wang XS, Dong Q, Fang JN, Li XY (2002) Structural features of immunologically active polysaccharides from Ganoderma lucidum. Phytochemistry 59:175–181

    PubMed  Article  CAS  Google Scholar 

  4. Bazzalo ME, Wright JE (1982) Survey of the Argentine species of the Ganoderma lucidum complex. Mycotaxon 16:295–325

    Google Scholar 

  5. Binder M, Larsson KH, Matheny PB, Hibbett DS (2010) Amylocorticiales ord. nov. and Jaapiales ord. nov.: Early-diverging clades of Agaricomycetidae were dominated by corticioid forms. Mycologia 102:865–880

    PubMed  Article  CAS  Google Scholar 

  6. Cao Y, Yuan HS (2012) Ganoderma mutabile sp. nov. from southwestern China based on morphological and molecular data. Mycol Progr. doi:10.1007/s11557-012-0819-9

  7. Dai YC (2010) Hymenochaetaceae (Basidiomycota) in China. Fungal Divers 45:131–343

    Article  Google Scholar 

  8. Dai YC (2012) Polypore diversity in China with an annotated checklist of Chinese polypores. Mycoscience 53:49–80

    Article  Google Scholar 

  9. Dai YC, Vainio EJ, Hantula J, Niemelä T, Korhonen K (2003) In vestigation on Heterobasidion annosum s.lat. in central and eastern Asia with the aid of mating tests and DNA fingerprinting. For Path 33:269–286

    Article  Google Scholar 

  10. Dai YC, Yang ZL, Cui BK, Yu CJ, Zhou LW (2009) Species diversity and utilization of medicinal mushrooms and fungi in China (Review). Int J Med Mushrooms 11:287–302

    Article  Google Scholar 

  11. De Silva DD, Rapior S, Fons F, Bahkali AH, Hyde KD (2012) Medicinal mushrooms in supportive cancer therapies: an approach to anti-cancer effects and putative mechanisms of action. Fungal Divers 55:1–35

    Article  Google Scholar 

  12. Felsenstein J (1985) Confidence intervals on phylogenetics: an approach using bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  13. Gao YH, Zhou SF (2003) Cancer prevention and treatment by Ganoderma, a mushroom with medicinal properties. Food Rev Int 19:275–325

    Article  Google Scholar 

  14. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes — application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    PubMed  Article  CAS  Google Scholar 

  15. Ge ZW, Yang ZL, Vellinga EC (2010) The genus Macrolepiota (Agaricaceae, Basidiomycota) in China. Fungal Divers 45:81–98

    Article  Google Scholar 

  16. Gilbertson RL, Ryvarden L (1986) North American Polypores 1. Fungiflora, Oslo, pp 1–433

    Google Scholar 

  17. Gottlieb AM, Wright JE (1999) Taxonomy of Ganoderma from southern South America: subgenus Ganoderma. Mycol Res 103:661–673

    Article  Google Scholar 

  18. Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704

    PubMed  Article  Google Scholar 

  19. Hall TA (1999) Bioedit: a user-friendly biological sequences alignment editor analysis program for windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  20. Hall BG (2004) Phylogenetic trees made easy: a how-to manual, 2nd edn. Sinauer Associates, Sunderland, pp 1–221

    Google Scholar 

  21. Hattori T, Ryvarden L (1994) Type studies in the Polyporaceae 25. Species described from Japan by R. Imazeki and A. Yasuda. Mycotaxon 50:27–46

    Google Scholar 

  22. He SH, Dai YC (2012) Taxonomy and phylogeny of Hymenochaete and allied genera of Hymenochaetaceae (Basidiomycota) in China. Fungal Divers. doi:10.1007/s13225-012-0174-9

  23. Hong SG, Jung HS (2004) Phylogenetic analysis of Ganoderma based on nearly complete mitochondrial small-subunit ribosomal DNA sequences. Mycologia 96:742–755

    PubMed  Article  Google Scholar 

  24. Hongo T, Izawa M (1994) Yama-Kei field books No.10. Yama-Kei Publishers Co., Ltd, Tokyo, pp 1–384, in Japanense

    Google Scholar 

  25. Hseu RS, Wang HH, Wang HF, Moncalvo JM (1996) Differentiation and grouping of isolates of the Ganoderma lucidum complex by random amplified polymorphic DNA-PCR compared with grouping on the basis of internal transcribed spacer sequences. Appl Environ Microbiol 62:1354–1363

    PubMed  CAS  Google Scholar 

  26. Hu H, Ahn NS, Yang XL, Lee YS, Kang KS (2002) Ganoderma lucidum extract induces cell cycle arrest and apoptosis in MCF-7 human breast cancer cell. Int J Cancer 102:250–253

    PubMed  Article  CAS  Google Scholar 

  27. Hyde KD, Bahkali AH, Moslem MA (2010) Fungi—an unusual source for cosmetics. Fungal Divers 43:1–9

    Article  Google Scholar 

  28. Jong SC, Birmingham JM (1992) Medicinal benefits of the mushroom Ganoderma. Adv Appl Microbiol 37:101–134

    PubMed  Article  CAS  Google Scholar 

  29. Kim HK, Seo GS, Kim HG (2001) Comparison of characteristics of Ganoderma lucidum according to geographical origins (II): consideration of morphological characteristics. Mycobiology 29:80–84

    Google Scholar 

  30. Kino K, Yamashita A, Yamaoka K, Watanabe J, Tanaka S, Ko K, Shimizu K, Tsunoo H (1989) Isolation and characterization of a new immunomodulatory protein, ling zhi-8 (LZ-8), from Ganoderma lucidium. J Biol Chem 264:472–478

    PubMed  CAS  Google Scholar 

  31. Lai T, Gao Y, Zhou SF (2004) Global marketing of medicinal Ling Zhi mushroom Ganoderma lucidum (W.Curt.:Fr.) Lloyd (Aphyllophoromycetideae) products and safety concerns. Int J Med Mushr 6:189–194

    Article  Google Scholar 

  32. Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759

    Article  CAS  Google Scholar 

  33. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    PubMed  Article  CAS  Google Scholar 

  34. Li YC, Yang ZL, Tolgor B (2009) Phylogenetic and biogeographic relationships of Chroogomphus species as inferred from molecular and morphological data. Fungal Divers 38:85–104

    Google Scholar 

  35. Lin ZB (2007) Modern Research of Ganoderma lucidum. Peking University Medical Press, Beijing, pp 1–359, in Chinese

    Google Scholar 

  36. Lin ZB (2009) Lingzhi: from mystery to science. Peking University Medical Press, Beijing, pp 1–162

    Google Scholar 

  37. Liu B (1974) The Chinese medical fungi. Shanxi People’s Press, Taiyuan, pp 1–196, in Chinese

    Google Scholar 

  38. Liu YL, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808

    PubMed  Article  CAS  Google Scholar 

  39. Mao XL (1998) Economic fungi of China. Science Press, Beijing, pp 1–762, in Chinese

    Google Scholar 

  40. Matheny PB, Liu YJ, Ammirati JF, Hall BD (2002) Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). Am J Bot 89:688–698

    PubMed  Article  CAS  Google Scholar 

  41. Matheny PB, Wang Z, Binder M, Curtis JM, Lim YW, Nilsson RH, Hughes KW, Petersen RH, Hofstetter V, Ammirati JF, Schoch C, Langer GE, McLaughlin DJ, Wilson AW, Crane PE, Frøslev T, Ge ZW, Kerrigan RW, Slot JC, Vellinga EC, Liang ZL, Aime MC, Baroni TJ, Fischer M, Hosaka K, Matsuura K, Seidl MT, Vaura J, Hibbett DS (2007) Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Mol Phylogenet Evol 43:430–451

    PubMed  Article  CAS  Google Scholar 

  42. Min BS, Gao JJ, Nakamura N, Hattori M (2000) Triterpenes from the spores of Ganoderma lucidum and their cytotoxicity against meth-A and LLC tumor cells. Chem Pharm Bull 48:1026–1033

    PubMed  Article  CAS  Google Scholar 

  43. Moncalvo JM, Ryvarden L (1997) A nomenclatural study of the Ganodermataceae Donk. Syn Fung 11:1–114

    Google Scholar 

  44. Moncalvo JM, Wang HF, Wang HH, Hseu RS (1994) The use of ribosomal DNA sequence data for species identification and phylogeny in the Ganodermataceae. In: Buchanan PK, Hseu RS, Moncalvo JM (eds) Ganoderma: systematics, phytopathology and pharmacology. Proceedings of contributed symposium 59A, B, 5th International Mycological Congress, Vancouver, August 14–21, 1994. National Taiwan University, Taipei, pp 31–44

  45. Moncalvo JM, Wang HF, Hseu RS (1995) Gene phylogeny of the Ganoderma lucidum complex based on ribosomal DNA sequences. Comparison with traditional taxonomic characters. Mycol Res 99:1489–1499

    Article  Google Scholar 

  46. Niemelä T, Miettinen O (2008) The identity of Ganoderma applanatum (Basidiomycota). Taxon 57:963–966

    Google Scholar 

  47. Núñez M, Ryvarden L (2000) East Asian polypores 1. Ganodermataceae and Hymenochaetaceae. Synop Fung 13:1–168

    Google Scholar 

  48. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  49. Patouillard N (1907) Champignons du Kouy-tcheou. Monde d be Pl. Seri. 2, 9: 31

  50. Pegler DN, Yao YJ (1996) Oriental species of Ganoderma section Ganoderma. In Wasser SP (ed). Botany and mycology for the next millenium: collection of scientific articles devoted to the 70th Anniversary of Academician Sytnik KM. Kyiv: Kholodny NG Institute of Botany, National Academy of Sciences of Ukraine. pp 336–347

  51. Petersen JH (1996) Farvekort. The Danish mycological society´s colour-chart. Foreningen til Svampekundskabens Fremme, Greve

  52. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    PubMed  Article  CAS  Google Scholar 

  53. Quanten E (1997) The polypores (Polyporaceae s.l.) of Papua New Guinea. Opera Bot Belgica 11:1–352

    Google Scholar 

  54. Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-a sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98

    PubMed  Article  CAS  Google Scholar 

  55. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    PubMed  Article  CAS  Google Scholar 

  56. Ryvarden L (1981) Type studies in the Polyporaceae. 12. Species described by F.W. Junghuhn. Persoonia 11:369–372

    Google Scholar 

  57. Ryvarden L (1983) Type studies in the Polyporaceae. 14. Species described by N. Patouillard, either alone or with other mycologists. Occas pap Farlow Herb 18:1–39

    Google Scholar 

  58. Ryvarden L (1985) Type studies in the Polyporaceae. 17. Species described by W. A. Murrill. Mycotaxon 23:169–198

    Google Scholar 

  59. Ryvarden L (1994) Can we trust morphology in Ganoderma? In: Buchanan PK, Hseu RS, Moncalvo JM (eds) Ganoderma: systematics, phytopathology and pharmacology. Proceedings of contributed symposium 59A, B, 5th International Mycological Congress, Vancouver, August 14–21, 1994. National Taiwan University, Taipei, pp 19–24

  60. Ryvarden L (2004) Neotropical polypores Part 1. Syn Fung 19:1–229

    Google Scholar 

  61. Ryvarden L, Gilbertson RL (1993) European polypores 1. Syn Fung 6:1–387

    Google Scholar 

  62. Ryvarden L, Johansen I (1980) A preliminary polypores flora of East Africa. Fungiflora, Oslo, pp 1–636

    Google Scholar 

  63. Sliva D, Labarrere C, Slivova V, Sedlak M, Lloyd FP Jr, Ho NWY (2002) Ganoderma lucidum suppresses motility of highly invasive breast and prostate cancer cells. Biochem Biophys Res Commun 298:603–612

    PubMed  Article  CAS  Google Scholar 

  64. Smith BJ, Sivasithamparam K (2000) Internal transcribed spacer ribosomal DNA sequence of five species of Ganoderma from Australia. Mycol Res 104:943–951

    Article  CAS  Google Scholar 

  65. Smith BJ, Sivasithamparam K (2003) Morphological studies of Ganoderma (Ganodermataceae) from the Australasian and Pacific regions. Aust Syst Bot 16:487–503

    Article  Google Scholar 

  66. Steyaert RL (1972) Species of Ganoderma and related genera mainly of the Bogor and Leiden Herbaria. Persoonia 7:55–118

    Google Scholar 

  67. Steyaert RL (1980) Study of some Ganoderma species. Bull Jard Bot Nat Belg 50:135–186

    Article  Google Scholar 

  68. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods) Version 4.0b10. Sinauer Associates, Sunderland

    Google Scholar 

  69. Szedlay G (2002) Is the widely used medicinal fungus the Ganoderma lucidum (fr.) karst. sensu stricto? Acta Microbiol Immunol Hung 49:235–243

    PubMed  Article  Google Scholar 

  70. Tai FL (1979) Sylloge fungorum sinicorum. Science Press, Beijing, pp 1–1527, in Chinese

    Google Scholar 

  71. Teng SC (1934) Notes on Polyporaceae from China. Sinensia 5:198–200

    Google Scholar 

  72. Wachtel-Galor WS, Tomlinson B, Benzie IFF (2004) Ganoderma lucidum (‘Lingzhi’), a Chinese medicinal mushroom: biomarker responses in a controlled human supplementation study. Brit J Nutr 91:263–269

    PubMed  Article  CAS  Google Scholar 

  73. Wang DM, Wu SH (2008) A taxonomic revision of the Ganodermataceae reported from Taiwan. Mycotaxon 104:297–308

    Google Scholar 

  74. Wang XC, Yao YJ (2009) Taxonomic studies on ‘Ganoderma lucidum’ in China. Abstracts of the 5th International Medicinal Mushroom Conference, Nantong, September 5–8, 2009. pp 104–106

  75. Wang DM, Wu SH, Li TH (2009a) Two records of Ganoderma new to mainland China. Mycotaxon 108:35–40

    Article  Google Scholar 

  76. Wang DM, Wu SH, Su CH, Peng JT, Shih YH, Chen LC (2009b) Ganoderma multipileum, the correct name for ‘G. lucidum’ in tropical Asia. Bot Stud 50:451–458

    Google Scholar 

  77. Wasser SP (2005) Reishi or Ling Zhi (Ganoderma lucidum). In: Coates PM, Blackman MR, Cragg GM, Levine M, Moss J, White JD (eds) Encyclopedia of dietary supplements. Marcel Dekker, New York, pp 603–622

    Google Scholar 

  78. Wasser SP (2011) Current findings, future trends, and unsolved problems in studies of medicinal mushrooms. Appl Microbiol Biotechnol 89:1323–1332

    PubMed  Article  CAS  Google Scholar 

  79. Wasser SP, Zmitrovich IV, Didukh MY, Spirin WA, Malysheva VF (2006) Morphological traits of Ganoderma lucidum complex highlighting G. tsugae var. jannieae: the current generalization. Gantner, Ruggell, pp 1–187

    Google Scholar 

  80. Welti S, Courtecuisse R (2010) The Ganodermataceae in the French West Indies (Guadeloupe and Martinique). Fungal Divers 43:103–126

    Article  Google Scholar 

  81. White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols, a guide to methods and applications. Academic, San Diego, pp 315–322

    Google Scholar 

  82. Wu XL, Dai YC (2005) Coloured illustrations of Ganodermataceae of China. Science Press, Beijing, pp 1–229, in Chinese

    Google Scholar 

  83. Yang ZL (2011) Molecular techniques revolutionize knowledge of basidiomycete evolution. Fungal Divers 50:47–58

    Article  Google Scholar 

  84. Ying JZ, Mao ZL, Ma QM, Zong LC, Wen HA (1987) Icons of medicinal fungi from China. Science Press, Beijing, pp 1–579, in Chinese

    Google Scholar 

  85. Yu YN, Shen MZ (2003) The history of Lingzhi (Ganoderma spp.) cultivation. Mycosystema 22:3–9, in Chinese

    Google Scholar 

  86. Zhang JS, Tang QJ, Zimmerman-Kordmann M, Reutter W, Fan H (2002) Activation of B lymphocytes by GLIS, a bioactive proteoglycan from Ganoderma lucidum. Life Sci 71:623–638

    PubMed  Article  CAS  Google Scholar 

  87. Zhao JD, Zhang XQ (2000) Flora Fungorum Sinicorum 18, Ganodermataceae. Science Press, Beijing, pp 1–204, in Chinese

    Google Scholar 

  88. Zhao RI, Desjardin DE, Soytong K, Perry BA, Hyde KD (2010) A monograph of Micropsalliota in Northern Thailand based on morphological and molecular data. Fungal Divers 45:33–79

    Article  Google Scholar 

  89. Zhao CL, Cui BK, Dai YC (2012) New species and phylogeny of Perenniporia based on morphological and molecular characters. Fungal Divers. doi:10.1007/s13225-012-0177-6

Download references

Acknowledgements

We thank Drs. T.Z. Wei and X.C. Wang (HMAS, China), Prof. L. Ryvarden and Dr. K.-H. Larsson (O, Norway) for loans of specimens. We are grateful to Prof. S. P. Wasser (UOH, Israel) for offering some important literatures and to CBS for offering some Ganoderma cutltures. We are indebted to Dr. D.M. Wang (GIM, China) and Dr. J.M. Moncalvo (ROM, Canada) for offering suggestions during this study. We appreciate Dr. H.S. Yuan (IFP, China) for improving the drawings, and Dr. S.H. He (BJFC, China) for offering some Ganoderma images. Y.C. Dai and S.H. Wu are deeply indebted to Dr. T. Niemelä (H, Finland) for his friendly support of their studies at Botanical Museum of the University of Helsinki. We are grateful to Prof. K.D. Hyde (Chiang Rai, Thailand) for improving the manuscript. The research was financed by the National Natural Science Foundation of China (Project Nos. 30910103907, 31070022).

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Sheng-Hua Wu or Yu-Cheng Dai.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cao, Y., Wu, SH. & Dai, YC. Species clarification of the prize medicinal Ganoderma mushroom “Lingzhi”. Fungal Diversity 56, 49–62 (2012). https://doi.org/10.1007/s13225-012-0178-5

Download citation

Keywords

  • Ganodermataceae
  • Ganoderma lingzhi
  • G. lucidum
  • Medicinal fungus
  • Phylogeny
  • Taxonomy